Published online before print July 24, 2003, 10.1148/radiol.2283021153
(Radiology 2003;228:629-634.)
© RSNA, 2003
Osseous Metastasis from Renal Cell Carcinoma: "Flow-Void" Sign at MR Imaging1
Jung-Ah Choi, MD,
Kyoung Ho Lee, MD,
Woo Sun Jun, MD,
Mi Gyung Yi, MD,
Sun Lee, MD and
Heung Sik Kang, MD
1 From the Department of Radiology, Seoul National University College of Medicine, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea; and the Institute of Radiation Medicine, SNUMRC (Seoul National University Medical Research Center), and Clinical Research Institute, Seoul National University Hospital, Korea (J.A.C., K.H.L., W.S.J., H.S.K.); Department of Radiology, Kumi Cha Hospital, Pochon Cha University, Kyoungsangbook-do, Korea (M.G.Y.); and Department of Pathology, National Cancer Center, Gyeonggi-do, Korea (S.L.). Received September 9, 2002; revision requested November 18; revision received December 3; accepted January 15, 2003. Address correspondence to H.S.K. (e-mail: kanghs@radcom.snu.ac.kr).
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ABSTRACT
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PURPOSE: To characterize the appearance and determine the importance of the "flow-void" sign on magnetic resonance (MR) images of patients with osseous metastasis from renal cell carcinoma.
MATERIALS AND METHODS: Three musculoskeletal radiologists retrospectively and independently reviewed the medical records of 16 patients who had undergone MR imaging and in whom 20 osseous metastatic lesions from renal cell carcinoma had been diagnosed on the basis of clinical and radiologic findings. They assessed the MR images for the presence and frequency of the flow-void sign—multiple dotlike or tubular structures with low signal intensity. They then compared these findings on MR images with the corresponding areas on available images obtained with radiography (n = 16), computed tomography (CT) (n = 6), and digital subtraction angiography (n = 3) and with the results of histopathologic analysis for the same patient group. They noted the location, diameter, and appearance of the lesion and the flow-void sign, as well as variations in signal intensity within the lesion and among lesions. Statistical analysis was performed to determine the level of interobserver agreement.
RESULTS: Radiographic findings and the level of signal intensity on MR images were nonspecific for diagnosis of osseous metastasis from renal cell carcinoma. The flow-void sign was identified at the lesion core or margin with a mean frequency of 76.7% by the three observers (in 15, 16, and 15 of 20 lesions, by observers 1, 2, and 3, respectively). Most of these areas of low signal intensity were tubular structures of less than 3 mm in diameter; in three lesions, they measured 5–8 mm in diameter. In 14 lesions, these structures corresponded to dilated blood vessels or veins identifiable on CT images (six lesions) or digital subtraction angiographic images (four lesions) or at histopathologic analysis (four lesions). The flow-void sign on MR images corresponded to vessels depicted on the CT scans available for six lesions and on the angiographic images available for four lesions.
CONCLUSION: Observation of the flow-void sign in lesions depicted on musculoskeletal MR images may prove helpful for diagnosing osseous metastasis from renal cell carcinoma and for treatment planning, especially in patients with occult or forgotten primary renal tumor.
© RSNA, 2003
Index terms: Bone neoplasms, MR, 30.12141, 40.12141 • Bone neoplasms, secondary, 30.33, 40.33 • Kidney neoplasms, 81.324
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INTRODUCTION
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Renal cell carcinoma (RCC) is known for its impressive metastatic potential (1–4) and must be considered in the differential diagnosis of any metastatic tumor (5). After the lung, bone is the second most common site of metastasis in patients with RCC, regardless of whether they underwent nephrectomy (2,4,6). Osseous metastasis occurs in 20%–60% of patients with RCC (4,7–9) and reportedly accounts for about 10% of pathologic fractures and 5% of instances of spinal cord compression in patients with RCC (10).
Because findings at radiography and magnetic resonance (MR) imaging in most bone lesions are nonspecific, diagnoses of osseous metastasis from RCC are usually based also on clinical information. It is difficult to diagnose metastatic RCC on the basis of imaging findings alone, because the metastasis may simulate a malignant primary bone tumor. The apparently solitary bone lesion may actually accompany an occult primary renal tumor, or it may be a delayed metastasis from a previously treated, forgotten primary lesion (9,11). Such circumstances are not uncommon in RCC.
RCC frequently manifests first as an osseous (often solitary) metastasis from a clinically occult primary tumor (5,11,14); this is the case in 48% of patients with osseous involvement of RCC (10) and in 4% of all patients with RCC (11). Solitary osseous metastases are relatively frequent, occurring in 2.5% of all patients with RCC (4,9,12–15). The most common site of solitary metastasis is the bone (4,8,12). One of the least understood aspects of RCC is the long quiescent period that may occur after initial diagnosis and treatment, followed by the sudden appearance of metastasis from an almost forgotten tumor. Although most metastases from RCC appear within 1–2 years after nephrectomy, bone metastases have manifested more than 20 years after the removal of the primary renal tumor, with no apparent disease in the interim (11).
We recently noticed a distinctive feature of osseous metastasis from RCC as depicted on MR images, a feature that we term the "flow-void" sign. This sign has not been described previously, to our knowledge. The purpose of this study was to characterize the appearance and determine the importance of the flow-void sign on MR images in osseous metastasis from RCC.
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MATERIALS AND METHODS
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Patients
The radiologic reports and clinical records of 59 patients with RCC who had undergone MR imaging at Seoul National University Hospital between January 1998 and October 2001 were reviewed. The institutional review board at our hospital did not require advance review of or informed consent for our retrospective study of patient records and images. We selected for inclusion in this study 16 patients (14 men and two women; age range, 54–87 years; average age, 67 years) with 20 lesions depicted on MR images and diagnosed as osseous metastasis from RCC. In 14 lesions (11 patients), the diagnosis had been confirmed with histopathologic analysis of tissue obtained from biopsy (ie, surgical excision or curettage) of the osseous lesion. In the remaining six lesions, osseous metastasis had been diagnosed on the basis of radiologic findings and prior histopathologic findings of RCC in a primary renal tumor. Diagnosis of RCC in the primary site had been confirmed with histopathologic analysis in all patients.
The clinical findings, including patient demographic information, site of osseous metastasis, and time interval between nephrectomy and osseous metastasis, were evaluated by one of two authors (J.A.C., K.H.L.).
Imaging
MR imaging was performed with either a 1.0-T magnet (Magnetom Expert; Siemens, Erlangen, Germany) or one of two 1.5-T magnets (Magnetom VP, Siemens; or Signa, GE Medical Systems, Milwaukee, Wis). MR images were obtained with either T2-weighted conventional spin-echo (SE) or fast SE pulse sequences (repetition time msec/echo time msec, 2,000–5,000/90–126; echo train length in fast SE imaging, nine to 29), as well as with T1-weighted conventional SE pulse sequences (400–660/12–15) performed before and after intravenous injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany). Images were obtained in at least three orthogonal planes for each patient and with section thicknesses of 3–10 mm.
Anteroposterior and lateral radiographs depicting all of the lesions, and contrast material–enhanced transverse computed tomographic (CT) scans acquired in six patients and depicting six osseous metastatic lesions, also were reviewed. In three patients (four lesions), digital subtraction angiography with anteroposterior, lateral, and both oblique views had been performed to define tumor vascularity and to guide subsequent transcatheter arterial embolization of the metastatic lesions.
All radiologic images analyzed in this study were acquired before surgical intervention, chemotherapy, transcatheter arterial embolization, or irradiation of the metastatic lesions.
Image Evaluation
Three experienced musculoskeletal radiologists (J.A.C., K.H.L., H.S.K.) retrospectively and independently reviewed the radiographs, MR images, CT scans, and digital subtraction angiographic images; all imaging results for a given patient were reviewed at the same time. Radiographs were evaluated with respect to lesion visibility, lytic or blastic nature, presence or absence of septa, and margins (ie, whether the margins were ill or well defined). MR images were assessed for lesion signal intensity and lesion diameter, as well as for the presence of the flow-void sign. Signal intensity in all lesions as depicted with the different pulse sequences was compared with the signal intensities of muscle and of fat and characterized as follows: Lesion signal intensity lower than signal intensity of muscle was described as "low"; the same as signal intensity of muscle, as "intermediate"; greater than signal intensity of muscle but less than signal intensity of fat, as "high"; and greater than signal intensity of fat, as "very high." The flow-void sign was defined as multiple dotlike or tubular structures with low signal intensity, located within or around the lesion, that probably corresponded to vessels. Unenhanced and contrast-enhanced transverse CT images were assessed for the presence of enhancing vessels, calcifications, and bone remnants in and around the lesion, and these findings were correlated with the flow-void sign observed on MR images. Angiographic images were reviewed to determine the extent of lesion vascularity and the pattern of vascular supply.
Efforts were made to trace the flow-void sign to adjacent, normal larger vessels. Findings on MR images were compared and correlated with vessels demonstrated on images from other modalities, such as CT and digital subtraction angiography, and at histopathologic analysis. The pathologic specimen slides were reviewed by a pathologist (S.L.) to determine histopathologic cell type and presence of endothelial cell–lined structures containing red blood cells.
Statistical Analysis
To obtain an objective indication of the frequency of occurrence of the flow-void sign, each of the three musculoskeletal radiologists independently recorded the presence or absence of the sign on the MR images. The resultant data were analyzed for interobserver agreement by using statistical software (SPSS, version 10.0; SPSS, Chicago, Ill) and in consultation with a statistician. The null hypothesis stated that 
equals zero; a statistic greater than 0.40 indicated good agreement, and a value greater than 0.75 indicated excellent agreement. A P value greater than .05 was considered to indicate statistically significant difference.
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RESULTS
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In six patients, diagnostic work-up including abdominal and chest CT, chest radiography, and bone scanning did not reveal any other metastatic lesion; therefore, the diagnosis was solitary osseous metastasis (Table 1). Six patients had osseous metastasis at initial manifestation of the disease; of these patients, four had solitary osseous metastasis. The time interval between nephrectomy and diagnosis of osseous metastasis in the other 10 patients ranged from 9 months to 14 years; it was 5 years or more in eight patients, and 10 years or more in three of these eight. In seven patients, osseous metastasis was the first metastasis diagnosed after nephrectomy; in two of these patients, the diagnosis was solitary osseous metastasis (Table 1).
The 18 metastases from RCC that were identified on radiographs were osteolytic lesions with ill-defined (15 lesions) or well-defined (three lesions) margins and without definable internal septa (Figs 1, 2). The remaining two lesions were not identifiable on radiographs (Table 1).
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Figure 1a. Images of the femur in a 61-year-old man with osseous metastasis from RCC. (a) Anteroposterior radiograph shows ill-defined osteolytic lesion (arrows) in the medial condyle. (b) Coronal T1-weighted MR image acquired with a conventional SE pulse sequence (450/14) shows a mass with intermediate signal intensity. Note the multiple dotlike or tubular structures of low signal intensity (arrows) inside and adjacent to the mass.
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Figure 1b. Images of the femur in a 61-year-old man with osseous metastasis from RCC. (a) Anteroposterior radiograph shows ill-defined osteolytic lesion (arrows) in the medial condyle. (b) Coronal T1-weighted MR image acquired with a conventional SE pulse sequence (450/14) shows a mass with intermediate signal intensity. Note the multiple dotlike or tubular structures of low signal intensity (arrows) inside and adjacent to the mass.
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Figure 2a. Images of the spine in a 54-year-old man with osseous metastasis from RCC. (a) Lateral radiograph shows an osteolytic lesion (arrows) in the L1 vertebral body. (b) Sagittal T1-weighted MR image acquired with a conventional SE pulse sequence (650/12) shows masses with intermediate signal intensity in the T12 and L1 vertebral bodies. Note the multiple dotlike or tubular structures (arrows) of low signal intensity inside these metastatic lesions, also seen in c. (c) Sagittal T2-weighted MR image obtained with a fast SE pulse sequence (650/12; echo train length, 15) shows hyperintense masses containing multiple dotlike or tubular structures (arrows). (d) Lateral selective digital subtraction angiographic image shows engorged vessels (arrows) with arteriovenous shunting in the L1 vertebral body.
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Figure 2b. Images of the spine in a 54-year-old man with osseous metastasis from RCC. (a) Lateral radiograph shows an osteolytic lesion (arrows) in the L1 vertebral body. (b) Sagittal T1-weighted MR image acquired with a conventional SE pulse sequence (650/12) shows masses with intermediate signal intensity in the T12 and L1 vertebral bodies. Note the multiple dotlike or tubular structures (arrows) of low signal intensity inside these metastatic lesions, also seen in c. (c) Sagittal T2-weighted MR image obtained with a fast SE pulse sequence (650/12; echo train length, 15) shows hyperintense masses containing multiple dotlike or tubular structures (arrows). (d) Lateral selective digital subtraction angiographic image shows engorged vessels (arrows) with arteriovenous shunting in the L1 vertebral body.
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Figure 2c. Images of the spine in a 54-year-old man with osseous metastasis from RCC. (a) Lateral radiograph shows an osteolytic lesion (arrows) in the L1 vertebral body. (b) Sagittal T1-weighted MR image acquired with a conventional SE pulse sequence (650/12) shows masses with intermediate signal intensity in the T12 and L1 vertebral bodies. Note the multiple dotlike or tubular structures (arrows) of low signal intensity inside these metastatic lesions, also seen in c. (c) Sagittal T2-weighted MR image obtained with a fast SE pulse sequence (650/12; echo train length, 15) shows hyperintense masses containing multiple dotlike or tubular structures (arrows). (d) Lateral selective digital subtraction angiographic image shows engorged vessels (arrows) with arteriovenous shunting in the L1 vertebral body.
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Figure 2d. Images of the spine in a 54-year-old man with osseous metastasis from RCC. (a) Lateral radiograph shows an osteolytic lesion (arrows) in the L1 vertebral body. (b) Sagittal T1-weighted MR image acquired with a conventional SE pulse sequence (650/12) shows masses with intermediate signal intensity in the T12 and L1 vertebral bodies. Note the multiple dotlike or tubular structures (arrows) of low signal intensity inside these metastatic lesions, also seen in c. (c) Sagittal T2-weighted MR image obtained with a fast SE pulse sequence (650/12; echo train length, 15) shows hyperintense masses containing multiple dotlike or tubular structures (arrows). (d) Lateral selective digital subtraction angiographic image shows engorged vessels (arrows) with arteriovenous shunting in the L1 vertebral body.
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At MR imaging, the metastatic lesions were 12–142 mm (average, 56 mm) in diameter (Table 1). They appeared as regions of high signal intensity (n = 18) or very high signal intensity (n = 2) on T2-weighted SE images and as regions of high signal intensity (n = 7), intermediate signal intensity (n = 12), or low signal intensity (n = 1) on T1-weighted SE images. On contrast-enhanced MR images, all lesions showed intense, solid enhancement, appearing as regions of high signal intensity (n = 19) or very high signal intensity (n = 1).
The flow-void sign was observed in 15 lesions (75%) by observer 1, 16 lesions (80%) by observer 2, and 15 lesions (75%) by observer 3 (Table 1). Good interobserver agreement was present, as indicated by the and P values obtained with statistical analysis (Table 2). The flow-void structures were traceable to normal larger vessels in 14 lesions. Although in most lesions these areas were tubular structures smaller than 3 mm in diameter, in three lesions (patients 6, 8, and 14) they were 5–8 mm in diameter.
Comparison of the available contrast-enhanced and unenhanced CT images (six lesions) with the corresponding MR images revealed that the structures with low signal intensity on MR images were dilated vessels, not areas in which the bone was being destroyed or displaced (Fig 3). All lesions on CT images were highly enhanced. The available digital subtraction angiographic images (four lesions) depicted hypervascular masses, with arteriovenous shunting in the arterial phase followed by intense contrast enhancement of the tumor. Multiple, enlarged, tortuous vessels also were observed in all lesions imaged with CT and/or digital subtraction angiography (Fig 3). Histopathologic analysis performed by a pathologist (S.L.) on tissue samples from 14 lesions confirmed hypervascular tumor of conventional clear cell type. In slices excised from the areas corresponding to flow-void structures observed on MR images, vascular tissue and red blood cells were especially predominant, surrounded by tubules and nests of cells with small nuclei set in abundant and clear cytoplasm.
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Figure 3a. Images of the chest in a 54-year-old man with osseous metastasis from RCC. (a) Anteroposterior radiograph shows the opacity of a large mass with destruction of the 5th rib on the patient’s right side. (b) Contrast-enhanced transverse CT image shows a mass near the chest wall. Note the tortuous vessels (arrows) inside the mass. (c) Transverse T1-weighted MR image acquired with a conventional SE sequence (550/12) shows a hyperintense mass. Note the multiple dotlike or tubular structures of low signal intensity (arrows) inside the lesions, also visible in d. (d) Contrast-enhanced coronal T1-weighted MR image acquired with a conventional SE sequence (594/15) shows enhancement in the mass and multiple dotlike or tubular structures of low signal intensity (arrows).
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Figure 3b. Images of the chest in a 54-year-old man with osseous metastasis from RCC. (a) Anteroposterior radiograph shows the opacity of a large mass with destruction of the 5th rib on the patient’s right side. (b) Contrast-enhanced transverse CT image shows a mass near the chest wall. Note the tortuous vessels (arrows) inside the mass. (c) Transverse T1-weighted MR image acquired with a conventional SE sequence (550/12) shows a hyperintense mass. Note the multiple dotlike or tubular structures of low signal intensity (arrows) inside the lesions, also visible in d. (d) Contrast-enhanced coronal T1-weighted MR image acquired with a conventional SE sequence (594/15) shows enhancement in the mass and multiple dotlike or tubular structures of low signal intensity (arrows).
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Figure 3c. Images of the chest in a 54-year-old man with osseous metastasis from RCC. (a) Anteroposterior radiograph shows the opacity of a large mass with destruction of the 5th rib on the patient’s right side. (b) Contrast-enhanced transverse CT image shows a mass near the chest wall. Note the tortuous vessels (arrows) inside the mass. (c) Transverse T1-weighted MR image acquired with a conventional SE sequence (550/12) shows a hyperintense mass. Note the multiple dotlike or tubular structures of low signal intensity (arrows) inside the lesions, also visible in d. (d) Contrast-enhanced coronal T1-weighted MR image acquired with a conventional SE sequence (594/15) shows enhancement in the mass and multiple dotlike or tubular structures of low signal intensity (arrows).
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Figure 3d. Images of the chest in a 54-year-old man with osseous metastasis from RCC. (a) Anteroposterior radiograph shows the opacity of a large mass with destruction of the 5th rib on the patient’s right side. (b) Contrast-enhanced transverse CT image shows a mass near the chest wall. Note the tortuous vessels (arrows) inside the mass. (c) Transverse T1-weighted MR image acquired with a conventional SE sequence (550/12) shows a hyperintense mass. Note the multiple dotlike or tubular structures of low signal intensity (arrows) inside the lesions, also visible in d. (d) Contrast-enhanced coronal T1-weighted MR image acquired with a conventional SE sequence (594/15) shows enhancement in the mass and multiple dotlike or tubular structures of low signal intensity (arrows).
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DISCUSSION
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Several investigators previously have defined the characteristic radiographic appearance of osseous metastases from RCC as osteolytic lesion with heavy or fine septa (9) or with a "hypervascular pattern" (16). Although such findings have been thought sufficiently distinctive to support a conclusion that RCC is the primary tumor (9), they are neither specific enough nor sensitive enough (9) and are no longer considered pathognomonic. In our experience, it is nearly impossible in most instances to make the diagnosis of metastatic RCC on the basis of radiologic findings without appropriate clinical information.
Although MR imaging is a well-established technique for evaluating bone and soft-tissue tumors, one of its main drawbacks is its relatively low specificity. MR imaging of metastatic tumors, including metastases from RCC, is no exception, and our analysis of lesion signal intensity on MR images in this study had variable results.
Yet, despite their nonspecificity, radiologic findings may prove useful in the establishment of a diagnosis of osseous metastasis from RCC and in subsequent treatment planning, especially when metastatic disease is confined to the osseous system, for the following reasons: First, radiologic indications of osseous metastasis from RCC can lead to a search for a hidden or forgotten primary tumor, which in many such cases is present (5,10,11,14). Second, localized treatments of osseous metastases, including surgery (3,6,8,10,17–19), radiation therapy (10), and percutaneous transcatheter arterial embolization (3,20), reportedly have been effective in relieving pain, preventing pathologic fractures, and improving patient mobility and function. Furthermore, aggressive surgical resection has been reported to prolong survival in patients with RCC, particularly those with metastatic lesions of relatively late onset (ie, 2 or more years after treatment of the primary tumor) in the appendicular skeletal structure (8,18).
Although our findings on MR images of at least three patients (patients 11, 13, and 16) were suggestive of metastatic RCC with occult primary renal tumor, the presence of low-signal-intensity areas in lesions depicted on MR images does not lead necessarily to a diagnosis of metastatic RCC. The flow-void sign merely represents relatively rapid blood flow through either dilated arteries supplying the hypervascular lesion or dilated veins draining the lesion. Various hypervascular musculoskeletal lesions have been described in the literature, including arteriovenous malformation, hemangioma, alveolar soft part sarcoma, synovial sarcoma, fibrosarcoma, chondroblastoma, giant cell tumor, osteoid osteoma, and aneurysmal bone cyst (16,21). Metastatic lesions from primary tumors other than RCC also have been reported to be hypervascular (20,22,23). The hypervascularity in most of those lesions was observed at angiography, however, and to our knowledge, areas of signal void on MR images of musculoskeletal lesions have been reported only in arteriovenous malformation, hemangioma with high blood flow, and alveolar soft part sarcoma (21,24–26). Our search of the literature for descriptions of areas of low signal intensity on MR images, particularly regarding patients with RCC, yielded disappointing results. To our knowledge, this sign has been described only in intracranial metastases (27) and in RCC tumor thrombus in the inferior vena cava (28).
Although the specificity of the flow-void sign for diagnosis of osseous metastasis from RCC is as yet unknown, its presence on MR images could aid in diagnosis and treatment planning by prompting a search for an occult or forgotten primary renal tumor or indicating a need for preoperative or palliative transcatheter arterial embolization. An important implication of the flow-void sign is its correlation with vessels; observation of this sign should alert the physician to proceed with caution when performing a biopsy or interventional procedure in the area of the lesion.
A major limitation of this study is that it did not determine the sensitivity and specificity of the flow-void sign for the diagnosis of metastatic RCC. Because study subjects were not consecutively enrolled and no hypervascular lesions were included other than osseous metastases from RCC, the presence and frequency of the flow-void sign in other tumors were not determined.
In conclusion, our study results indicate that the numerous dotlike or tubular structures of low signal intensity observed on MR images of osseous metastases from RCC represent dilated vessels supplying or draining the tumor. Although the diagnostic sensitivity and specificity of what we term the "flow-void" sign have yet to be determined, an awareness of the implications of this sign may be helpful in suggesting a diagnosis and a treatment plan, especially in patients who have occult or forgotten primary renal tumor.
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FOOTNOTES
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Abbreviations: RCC = renal cell carcinoma,
SE = spin-echo
Author contributions: Guarantor of integrity of entire study, H.S.K.; study concepts, S.L., J.A.C., M.G.Y.; study design, K.H.L., W.S.J.; literature research, W.S.J.; clinical studies, J.A.C., K.H.L.; data acquisition, J.A.C., K.H.L.; data analysis/interpretation, K.H.L., H.S.K.; statistical analysis, K.H.L., J.A.C.; manuscript preparation, J.A.C., W.S.J.; manuscript definition of intellectual content, K.H.L., M.G.Y.; manuscript editing, J.A.C., H.S.K.; manuscript revision/review, J.A.C., S.L., H.S.K.; manuscript final version approval, all authors
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ABSTRACT
INTRODUCTION
